Prospective application of clinician-performed lung ultrasonography during the 2009 H1N1 influenza A pandemic: distinguishing viral from bacterial pneumonia
© Tsung et al.; licensee Springer. 2012
Received: 6 May 2012
Accepted: 14 June 2012
Published: 10 July 2012
Emergency department visits quadrupled with the initial onset and surge during the 2009 H1N1 influenza pandemic in New York City from April to June 2009. This time period was unique in that >90% of the circulating virus was surveyed to be the novel 2009 H1N1 influenza A according to the New York City Department of Health. We describe our experience using lung ultrasound in a case series of patients with respiratory symptoms requiring chest X-ray during the initial onset and surge of the 2009 H1N1 influenza pandemic.
We describe a case series of patients from a prospective observational cohort study of lung ultrasound, enrolling patients requiring chest X-ray for suspected pneumonia that coincided with the onset and surge of the 2009 H1N1 influenza pandemic.
Twenty pandemic 2009 H1N1 influenza patients requiring chest X-ray were enrolled during this time period. Median age was 6.7 years. Lung ultrasound via modified Bedside Lung Ultrasound in Emergency protocol assisted in the identification of viral pneumonia (n = 15; 75%), viral pneumonia with superimposed bacterial pneumonia (n = 7; 35%), isolated bacterial pneumonia only (n = 1; 5%), and no findings of viral or bacterial pneumonia (n = 4; 20%) in this cohort of patients. Based on 54 observations, interobserver agreement for distinguishing viral from bacterial pneumonia using lung ultrasound was ĸ = 0.82 (0.63 to 0.99).
Lung ultrasound may be used to distinguish viral from bacterial pneumonia. Lung ultrasound may be useful during epidemics or pandemics of acute respiratory illnesses for rapid point-of-care triage and management of patients.
KeywordsUltrasound H1N1 virus Pneumonia Emergency medicine Point-of-care Pandemic Pediatric
This fourfold increase in patient volume presented logistical challenges for emergency departments . In response to mass casualty incident-type conditions and overcrowding, emergency departments in New York City added staffing and created alternate sites of care to accommodate the increased patient volume. Increased demand for chest radiography for those patients with more severe disease led to increased delays and length of stay for those patients with suspected, but non-severe pneumonia.
Study design and setting
We describe a subcohort of patients who required chest X-ray for suspected pneumonia and were enrolled into a prospective study of lung ultrasound for diagnosing pneumonia that coincided with the onset and surge of the 2009 H1N1 influenza pandemic from April to June 2009 [1, 2, 13]. We also describe the application of a modified Bedside Lung Ultrasound in Emergency (BLUE) protocol  with posterior thorax scanning (Figure 3) during the onset and surge of pandemic patients in an urban emergency department.
This study was approved by our institutional review board. The study population consisted of a convenience sample of patients who met predetermined inclusion criteria and in whom informed consent had been obtained and documented from the patient or guardian for enrollment into the study.
Selection of participants
Inclusion criteria consisted of patients < 21 years of age presenting to the emergency department with clinical suspicion of pneumonia requiring chest X-ray for evaluationWe excluded those patients who presented the following: (1) arrival in the emergency department with a chest X-ray, (2) a confirmed diagnosis of pneumonia by diagnostic imaging, or (3) hemodynamic instability.
Methods of measurement and outcome measures
Additional file 1: Title: Small subpleural consolidation. Description: Small subpleural consolidation consistent with viral lung ultrasound pattern. (MOV )
Additional file 2: Title: Confluent B-lines. Description: Confluent B-lines consistent with viral lung ultrasound pattern. (MOV )
Additional file 3: Title: Rt anterior middle lobe lung consolidation with air bronchograms. Description:Rt anterior middle lobe lung consolidation with air bronchograms consistent with bacterial pneumonia lung ultrasound pattern. (MOV )
Ultrasound images and videos were reviewed between two blinded investigator sonologists (enrolling sonologist and reviewing sonologist) to determine interobserver agreement by unweighted Cohens Kappa for viral pneumonia (small subpleural consolidation and/or B-lines), normal lung ultrasound pattern (A-lines), and bacterial pneumonia (lung consolidation with sonographic air bronchograms).
Characteristics of study subjects
6.7 years (IQR, 3.6 to 10.7)
Median US exam time (IQR)
6 min (IQR, 4 to 8)
History of fever
History of cough
Median time to CXR from request prior to pandemic (N = 20)
29 min (IQR, 18 to 43)
Median time to CXR from request during pandemic surge (N = 20)
98 min (IQR, 79 to 125)
Findings ( N = 20)
US - n ; % [95% CI]
CXR - n ; % [95% CI]
15; 75 [53 to 89]
8; 40 [22 to 61]
Bacterial pneumonia only
1; 5 [0 to 25]
5; 25 [11 to 47]
Antibiotics and oseltamivir
Viral and bacterial pneumonia
7; 35 [18 to 59]
3; 15 [3 to 38]
Antibiotics and oseltamivir
4; 20 [7 to 42]
7; 35 [18 to 59]
Discharge and observation
Cohen’s Kappa for distinguishing viral from bacterial pneumonia on lung ultrasound between two blinded sonologists
Cohen’s Kappa = 0.82
95% CI (0.63 to 0.99)
Additional file 4: Title: Confluent B-lines and lung consolidation with air bronchograms. Description: Viral and bacterial pneumonia lung ultrasound patterns. (MOV )
All patients in our series were recovering or recovered from their influenza illness on follow-up after 2 weeks. All admitted patients were subsequently confirmed with the 2009 H1N1 influenza A by the New York City Department of Health. Per hospital protocol for possible hospital admission, four of nine patients tested positive for influenza A by viral antigen testing, despite the New York City Department of Health reporting >90% of the circulating virus during this pandemic time period was the novel influenza A H1N1 . One infant in the cohort was co-infected with respiratory syncytial virus based on viral antigen testing. Three patients, all <5 years of age requiring hospital admission had evidence of both bacterial and viral pneumonia on ultrasound. The only patient requiring ICU admission, a 20-year-old female, was intubated after deteriorating during her ED stay with persistent hypotension and septic shock from a left lower lobe bacterial pneumonia. This patient initially presented with an influenza-like illness and acute abdominal pain.
To our knowledge, this is the first prospective series describing the use of lung ultrasound in children as a potential real-time diagnostic triage tool during a mass casualty-type incident due to an acute respiratory illness pandemic surge [17, 18]. Testa et al. have reported on similar lung ultrasound findings in adults during the 2009 H1N1 influenza A pandemic . Single case reports of clinician-performed lung ultrasound to monitor the progression of H1N1 influenza-associated ARDS  and point-of-care echocardiography to diagnose H1N1 influenza myocarditis  have been described. Retrospective reports of the role of ultrasound in mass casualty incidents during disasters such as earthquakes have also been described [21, 22]. Lichtenstein et al. described an algorithm using lung ultrasonography to distinguish between various respiratory pathologies of the lung . We modified Lichtenstein’s BLUE protocol  to recognize basic lung ultrasound patterns to distinguish between the normal unaffected lung, viral pneumonia pattern, and bacterial pneumonia (Figure 3). Scanning the posterior thorax was added to increase the sensitivity of the protocol . Point-of-care lung ultrasound was able to identify, in real-time, four groups of pandemic patients: viral pneumonia only (subpleural consolidations and/or B-lines or confluent B-lines), bacterial pneumonia only (lung consolidation with sonographic air bronchograms), both viral and bacterial pneumonia (Figure 7), and normal lungs (A-lines only). Our calculated Kappa was 0.82, which means that the interobserver agreement in distinguishing between these ultrasound findings was excellent.
These ultrasound findings facilitated triage and immediate decision making regarding the need for respiratory isolation in a negative pressure room without waiting for chest X-ray. Our median time to chest X-ray tripled (Table 1) during the pandemic compared to a time period prior to the pandemic. Our time to chest X-ray interpretation during the pandemic was longer than the median of 98 min reported by Zanobetti et al. in the study of emergency department lung ultrasound in non-pandemic conditions .
When lung consolidation with sonographic air bronchograms was visualized, point-of-care ultrasound facilitated the immediate decision to treat with antibiotics, without waiting for chest X-ray. Visualization of viral pneumonia on ultrasound may be useful to assist in the decision to initiate immediate empiric treatment with antiviral medication for future pandemic or epidemic influenza patients. In a large cohort of hospitalized H1N1 influenza A pandemic patients, only 73% of patients with radiographic evidence of pneumonia received antiviral drugs, whereas 97% received antibiotics . Better recognition of viral pneumonia by ultrasound may impact outcomes, as available data have shown treatment with antiviral medication reduces mortality in hospitalized patients with influenza, even when therapy is initiated after 48 h of illness onset .
Our sample size was limited by the inability to enroll during the surge of pandemic patients due to time and resource constraints. Selection bias from convenience sampling may have occurred because patients were more likely to have been enrolled at less busier or better staffed times. In general, the patients in this series had illnesses severe enough to warrant investigation with chest X-ray. Thus, information about less ill or asymptomatic pandemic patients is lacking.
Although our calculated interobserver agreement for lung ultrasound to distinguish between viral and bacterial pneumonia is high, the number of total observations was limited, and this is reflected in our wide 95% confidence intervals. However, it is notable that our point estimate Kappa for ultrasound is higher than the reported interobserver agreement for chest X-ray for pneumonia by pediatric radiologists, 0.51 (0.39 to 0.64) .
Due to the large numbers of patients presenting to our emergency department during the pandemic, only hospitalized patients (four patients in our series) were confirmed with 2009 H1N1 influenza A . Finding small subpleural consolidations and/or B-lines on ultrasound allows the recognition of viral pneumonia from bacterial pneumonia (lung consolidation with sonographic air bronchograms), but it is unknown if different viruses have unique lung ultrasound patterns (e.g., influenza A from RSV). We could not report test performance characteristics, such as sensitivity and specificity, as there was no practical reference gold standard for viral pneumonia at the time our study was conducted. Additionally, chest X-ray cannot be used as a gold standard for viral pneumonia. However, according to the New York City Department of Health, >90% of the circulating virus during this pandemic time period was the novel influenza A H1N1 .
Lung ultrasound may be used to distinguish viral from bacterial pneumonia with high interobserver agreement. Lung ultrasonography may be useful during epidemics or pandemics of acute respiratory illnesses for rapid point-of-care triage and management of patients.
JWT and VPS participated in the design of the study, coordinated the study, and performed the statistical analysis. JWT, DOK, and VPS participated in the patient enrollment and data collection and drafting of the manuscript. All authors read and approved the final manuscript.
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